Humanization of wildlife gut microbiota in urban environments

Urbanization is rapidly altering Earth’s environments, demanding investigations of the impacts on resident wildlife. Here, we show that urban populations of coyotes (Canis latrans) and crested anole lizards (Anolis cristatellus) acquire gut microbiota constituents found in humans, including the gut bacterial lineages most significantly associated with urbanization in humans (e.g., Bacteroides). Comparisons of urban and rural wildlife and human populations revealed significant convergence of the gut microbiota among urban host populations. Remarkably, all microbial lineages found in humans that were overrepresented in urban wildlife relative to rural wildlife were also overrepresented in urban humans relative to rural humans. These results indicate parallel effects of urbanization on human and wildlife gut microbiota and suggest spillover of bacteria from humans into wildlife in cities.

Comparative Study of the Gut Microbiota Among Four Different Marine Mammals in an Aquarium

Despite an increasing appreciation in the importance of host–microbe interactions in ecological and evolutionary processes, information on the gut microbial communities of some marine mammals is still lacking. Moreover, whether diet, environment, or host phylogeny has the greatest impact on microbial community structure is still unknown. To fill part of this knowledge gap, we exploited a natural experiment provided by an aquarium with belugas (Delphinapterus leucas) affiliated with family Monodontidae, Pacific white-sided dolphins (Lagenorhynchus obliquidens) and common bottlenose dolphin (Tursiops truncatus) affiliated with family Delphinidae, and Cape fur seals (Arctocephalus pusillus pusillus) affiliated with family Otariidae. Results show significant differences in microbial community composition of whales, dolphins, and fur seals and indicate that host phylogeny (family level) plays the most important role in shaping the microbial communities, rather than food and environment. In general, the gut microbial communities of dolphins had significantly lower diversity compared to that of whales and fur seals. Overall, the gut microbial communities were mainly composed of Firmicutes and Gammaproteobacteria, together with some from Bacteroidetes, Fusobacteria, and Epsilonbacteraeota. However, specific bacterial lineages were differentially distributed among the marine mammal groups. For instance, Lachnospiraceae, Ruminococcaceae, and Peptostreptococcaceae were the dominant bacterial lineages in the gut of belugas, while for Cape fur seals, Moraxellaceae and Bacteroidaceae were the main bacterial lineages. Moreover, gut microbial communities in both Pacific white-sided dolphins and common bottlenose dolphins were dominated by a number of pathogenic bacteria, including Clostridium perfringens, Vibrio fluvialis, and Morganella morganii, reflecting the poor health condition of these animals. Although there is a growing recognition of the role microorganisms play in the gut of marine mammals, current knowledge about these microbial communities is still severely lacking. Large-scale research studies should be undertaken to reveal the roles played by the gut microbiota of different marine mammal species.

Microbial Communities of the Hydrothermal Scaly-Foot Snails From Kairei and Longqi Vent Fields

The microbial communities of the hydrothermal Scaly-foot Snails (SFSs) from independent hydrothermal vent fields have not been investigated in depth. In this study, we collected SFSs from two different hydrothermal environments located on the Central Indian Ridge (CIR) and the Southwest Indian Ridge (SWIR), the Kairei and Longqi vent fields, respectively. Additionally, one SFS collected from the Kairei vent field was reared for 16 days with in situ deep-sea seawater. The epibiotic and internal samples of SFSs, including ctenidium, esophageal gland, visceral mass, shells, and scales, were examined for microbial community compositions based on the 16S rRNA gene. Our results revealed significant differences in microbial community composition between SFSs samples collected from Kairei and Longqi vent fields. Moreover, the microbial communities of epibiotic and internal SFS samples also exhibited significant differences. Epibiotic SFS samples were dominated by the bacterial lineages of Sulfurovaceae, Desulfobulbaceae, Flavobacteriaceae, and Campylobacteraceae. While in the internal SFS samples, the genus Candidatus Thiobios, affiliated with the Chromatiaceae, was the most dominant bacterial lineage. Furthermore, the core microbial communities of all samples, which accounted for 78 ∼ 92% of sequences, were dominated by Chromatiaceae (27 ∼ 49%), Sulfurovaceae (10 ∼ 35%), Desulfobulbaceae (2 ∼ 7%), and Flavobacteriaceae (3 ∼ 7%) at the family level. Based on the results of random forest analysis, we also found the genera Desulfobulbus and Sulfurovum were the primary bacterial lineages responsible for the dissimilarity of microbial communities between the SFS samples collected from the Kairei and Longqi vent fields. Our results indicated that the microbial lineages involved in the sulfur cycle were the key microorganisms, playing a crucial role in the hydrothermal vent ecosystems. Our findings expand current knowledge on microbial diversity and composition in the epibiotic and internal microbial communities of SFS collected from different hydrothermal vent fields.

Novel strain-level resolution of Crohn’s disease mucosa-associated microbiota via an ex vivo combination of microbe culture and metagenomic sequencing

The mucosa-associated microbiota is widely recognized as a potential trigger for Crohn’s disease pathophysiology but remains largely uncharacterised beyond its taxonomic composition. Unlike stool microbiota, the functional characterisation of these communities using current DNA/RNA sequencing approaches remains constrained by the relatively small microbial density on tissue, and the overwhelming amount of human DNA recovered during sample preparation. Here, we have used a novel ex vivo approach that combines microbe culture from anaerobically preserved tissue with metagenome sequencing (MC-MGS) to reveal patient-specific and strain-level differences among these communities in post-operative Crohn’s disease patients. The 16 S rRNA gene amplicon profiles showed these cultures provide a representative and holistic representation of the mucosa-associated microbiota, and MC-MGS produced both high quality metagenome-assembled genomes of recovered novel bacterial lineages. The MC-MGS approach also produced a strain-level resolution of key Enterobacteriacea and their associated virulence factors and revealed that urease activity underpins a key and diverse metabolic guild in these communities, which was confirmed by culture-based studies with axenic cultures. Collectively, these findings using MC-MGS show that the Crohn’s disease mucosa-associated microbiota possesses taxonomic and functional attributes that are highly individualistic, borne at least in part by novel bacterial lineages not readily isolated or characterised from stool samples using current sequencing approaches.

Evolution of Interbacterial Antagonism in Bee Gut Microbiota Reflects Host and Symbiont Diversification

ABSTRACT Gram-negative bacteria frequently possess type VI secretion systems (T6SSs), protein complexes that are able to inject toxic proteins into nearby cells. Many aspects of T6SS structure and function have been characterized for model species, but less is known about the evolutionary processes that shape T6SS and effector (toxin) diversity in host-associated microbial communities. The bee gut microbiota is a simple community that has codiversified with bees for >80 million years. This study investigated how complements of T6SSs and effectors within the bee microbiota changed as bacteria and their hosts diversified into isolated species. We used protein homology to survey 198 isolate genomes of 9 Gram-negative species for genes encoding T6SS structural components; Rhs toxins, which are common T6SS effectors; and VgrG proteins, which are structural components associated with specific toxins. T6SS loci were present in 5 species clusters found only in bees, namely Apibacter spp., Gilliamella spp., Frischella perrara, “Candidatus Schmidhempelia bombi,” and Snodgrassella alvi. The distribution of T6SS loci suggests that at least 3 were present in the microbiota of the common ancestor of social bees and that loss of these genes in some bacterial lineages was linked to both host and bacterial speciation. Isolates differed enormously in repertoires of Rhs and VgrG proteins. We found that bacterial species employ different mechanisms for toxin acquisition and diversification and that species and strains sometimes lose the T6SS entirely, likely causing shifts in competitive dynamics within these communities. IMPORTANCE Antagonistic interactions between bacteria affect diversity and dynamics of host-associated communities, including gut communities that are linked to host health. In many bacterial communities, including human and honey bee gut microbiotas, antagonism is mediated by type VI secretion systems (T6SSs) that deliver lethal toxins to competing strains. In this study, we explored how T6SSs and associated toxins have evolved in the simple, host-specific gut microbiota of honey bees and bumble bees. Using comparative genomics, we explored the conservation, recombination, horizontal transfer, and loss of T6SSs and effectors during 80 million years of evolution of this bee-associated community. We find that that patterns of T6SS loss and retention are linked to differences in biology across host species, while trends in effector diversification are mostly specific to bacterial lineages.

Microbial trait evolution is dominated by frequent and rare pulsed evolution

On the macroevolutionary timescale, does trait evolution proceed gradually or by rapid bursts (pulses) separated by long periods of stasis? Although studies have shown pulsed evolution is prevalent in animals, our knowledge about the tempo and mode of evolution across the tree of life is very limited. This long-standing debate calls for a test in bacteria and archaea, the most ancient and diverse forms of life with unique population genetic properties. Using a likelihood-based framework, we analyzed patterns of microbial genomic trait evolution on a broad macroevolutionary timescale. Here we show that pulsed evolution is both prevalent and predominant in microbes. For the first time, we detected two distinct types of pulsed evolution that are predicted by the punctuated equilibrium and quantum evolution theories. Our findings suggest that major bacterial lineages originated in quick bursts and pulsed evolution is common across the tree of life despite drastically different population genetic properties of animals, plants and microbes.

Evolutionary jumps in bacterial GC content

The diversity of bacterial GC content (ranging from 13-75%) has been studied for many decades, yet its evolution remains incompletely understood. Since it is difficult to observe GC content evolve on realistic time scales in the laboratory, comparative approaches are instrumental for its study. Additionally, investigating phylogenetic patterns in a trait’s diversity can provide greater insight into its evolution; but this dimension is rarely studied systematically in the case of bacterial GC content. Therefore, we applied phylogenetic models – typically used for studying morphological or behavioral traits of animals and plants – to the study of this fundamental molecular trait. We find that GC content diversifies via a combination of gradual evolution and evolutionary “jumps” in multiple bacterial groups across two major bacterial phyla. In a systematic survey of these GC content jumps, we retrieved many well-studied cases of severe evolutionary reduction in GC content of endosymbiotic bacteria, but also identified GC content jumps in bacterial lineages beyond such peculiar contexts. Surprisingly, unlike prior reports that solely focused on reductions in GC, we found a comparable number of jumps with both increased and decreased GC content. Our preliminary analysis of potential ecological explanations of GC jumps suggests that most of these GC jumps are not concomitant with changes in previously implicated factors such as host association or oxygen dependence. Thus, the ecological and evolutionary drivers of rapid and large shifts in GC content remain open questions. Our systematic identification of bacterial lineages experiencing GC jumps provides new datasets and novel contexts to address these questions.

Novel enzyme for dimethyl sulfide-releasing in bacteria reveals a missing route in the marine sulfur cycle

Dimethylsulfoniopropionate (DMSP) is an abundant and ubiquitous organosulfur molecule and plays important roles in the global sulfur cycle. Cleavage of DMSP produces volatile dimethyl sulfide (DMS), which has impacts on the global climate. Multiple pathways for DMSP catabolism have been identified. Here we identified yet another novel pathway, the ATP DMSP lysis pathway. The key enzyme, AcoD, is an ATP-dependent DMSP lyase. AcoD belongs to the acyl-CoA synthetase superfamily, which is totally different from other DMSP lyases, showing a new evolution route. AcoD catalyses the conversion of DMSP to DMS by a two-step reaction: the ligation of DMSP with CoA to form the intermediate DMSP-CoA, which is then cleaved to DMS and acryloyl-CoA. The novel catalytic mechanism was elucidated by structural and biochemical analyses. AcoD is widely distributed in many bacterial lineages including Alphaproteobacteria, Betaproteobacteria, Gammaproteobacteria and Firmicutes, revealing this new pathway plays important roles in global DMSP/DMS cycles.